skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Listening to your partner: serotonin increases male responsiveness to female vocal signals in mice
The context surrounding vocal communication can have a strong influence on how vocal signals are perceived. The serotonergic system is well-positioned for modulating the perception of communication signals according to context, because serotonergic neurons are responsive to social context, influence social behavior, and innervate auditory regions. Animals like lab mice can be excellent models for exploring how serotonin affects the primary neural systems involved in vocal perception, including within central auditory regions like the inferior colliculus (IC). Within the IC, serotonergic activity reflects not only the presence of a conspecific, but also the valence of a given social interaction. To assess whether serotonin can influence the perception of vocal signals in male mice, we manipulated serotonin systemically with an injection of its precursor 5-HTP, and locally in the IC with an infusion of fenfluramine, a serotonin reuptake blocker. Mice then participated in a behavioral assay in which males suppress their ultrasonic vocalizations (USVs) in response to the playback of female broadband vocalizations (BBVs), used in defensive aggression by females when interacting with males. Both 5-HTP and fenfluramine increased the suppression of USVs during BBV playback relative to controls. 5-HTP additionally decreased the baseline production of a specific type of USV and male investigation, but neither drug treatment strongly affected male digging or grooming. These findings show that serotonin modifies behavioral responses to vocal signals in mice, in part by acting in auditory brain regions, and suggest that mouse vocal behavior can serve as a useful model for exploring the mechanisms of context in human communication.  more » « less
Award ID(s):
1856436
PAR ID:
10538897
Author(s) / Creator(s):
;
Corporate Creator(s):
Editor(s):
Nagarajan, SS; Turner, JA
Publisher / Repository:
Frontiers Media SA
Date Published:
Journal Name:
Frontiers in Human Neuroscience
Edition / Version:
1
Volume:
17
Issue:
na
ISSN:
1662-5161
Page Range / eLocation ID:
1304653
Subject(s) / Keyword(s):
USV courtship inferior colliculus serotonin squeak vocalization
Format(s):
Medium: X Size: na Other: PDF/A
Size(s):
na
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; (, PLOS ONE)
    Coleman, Melissa J. (Ed.)
    Although male vocalizations during opposite- sex interaction have been heavily studied as sexually selected signals, the understanding of the roles of female vocal signals produced in this context is more limited. During intersexual interactions between mice, males produce a majority of ultrasonic vocalizations (USVs), while females produce a majority of human-audible squeaks, also called broadband vocalizations (BBVs). BBVs may be produced in conjunction with defensive aggression, making it difficult to assess whether males respond to BBVs themselves. To assess the direct effect of BBVs on male behavior, we used a split-cage paradigm in which high rates of male USVs were elicited by female presence on the other side of a barrier, but which precluded extensive male-female contact and the spontaneous production of BBVs. In this paradigm, playback of female BBVs decreased USV production, which recovered after the playback period. Trials in which female vocalizations were prevented by the use of female bedding alone or of anesthetized females as stimuli also showed a decrease in response to BBV playback. No non-vocal behaviors declined during playback, although digging behavior increased. Similar to BBVs, WNs also robustly suppressed USV production, albeit to a significantly larger extent. USVs suppression had two distinct temporal components. When grouped in 5-second bins, USVs interleaved with bursts of stimulus BBVs. USV suppression also adapted to BBV playback on the order of minutes. Adaptation occurred more rapidly in males that were housed individually as opposed to socially for a week prior to testing, suggesting that the adaptation trajectory is sensitive to social experience. These findings suggest the possibility that vocal interaction between male and female mice, with males suppressing USVs in response to BBVs, may influence the dynamics of communicative behavior. 
    more » « less
  2. ; ; ; (, Journal of Neurophysiology)
    Past social experience and current social context shape the responses of animals to social signals. The serotonergic system is one potential mechanism by which both experiential and contextual factors could be conveyed to sensory systems, such as the auditory system, for multiple reasons. 1) Many features of the serotonergic system are sensitive to social experience. 2) Elevations in serotonergic activity are triggered by social partners, and variations in socially triggered serotonergic responses reflect behavioral differences among social encounters. 3) Serotonin is an auditory neuromodulator, altering how auditory neurons respond to sounds including conspecific vocalizations. In this study, we tested how social experience influences the socially triggered serotonergic response in the inferior colliculus, an auditory midbrain region with an important role in vocalization processing. We used carbon fiber voltammetry to measure serotonin during social interactions of male mice ( Mus musculus) from different social backgrounds: 4 weeks of grouped or individual housing. When paired with an unfamiliar male, both group-housed and individually housed males demonstrated elevations in serotonin; however, individually housed males exhibited socially triggered serotonergic responses with delayed time courses compared with the group-housed males. Furthermore, group-housed males displayed previously described correlations between the socially triggered serotonergic response and behaviors such as social investigation. In contrast, individually housed males did not show these serotonin-behavior relationships. These results suggest that social experience gained via social housing may shape the ability of the central serotonergic system to encode social context in sensory regions. NEW & NOTEWORTHY We demonstrate that past social experience influences the fidelity with which the serotonergic system represents social context in an auditory region. Social experience altered the time course of socially triggered serotonergic responses and changed how the serotonergic system reflects behavioral variations among social encounters of the same context. These findings are significant to the study of communication, suggesting that centralized neuromodulatory systems potentially convey integrated information regarding past experience and current context to primary sensory regions. 
    more » « less
  3. ; ; (, Integrative and Comparative Biology)
    null (Ed.)
    Abstract Juvenile social experience, such as social isolation, has profound effects on communicative behavior, including signal production and reception. In the current study, we explored responsiveness to the neuromodulator serotonin as a potential mechanistic link between early life social isolation and auditory processing. The serotonergic system is sensitive to social isolation in many brain regions including the inferior colliculus (IC), an auditory midbrain nucleus. We investigated the effects of social experience on serotonergic responsiveness by measuring cFos, an immediate early gene product, in the IC of female mice. Serotonin was manipulated pharmacologically by administering fenfluramine, pCPA, or saline to mice that had undergone an extreme dichotomy in social experience after weaning: being housed in social groups versus individually. These mice were exposed to a 60-min recording of vocalizations from an opposite-sex interaction and perfused. Using immunohistochemistry, we measured the density of cFos-positive (cFos+) nuclei in the major subdivisions of the IC. Housing condition, drug treatment, and IC subregion all had a significant effect on cFos+ density. The central IC showed the highest density of cFos+ cells and also the most pronounced effects of housing condition and drug treatment. In the central IC, cFos+ density was higher following fenfluramine treatment than saline, and lower following pCPA treatment than fenfluramine. Individually housed mice showed a higher cFos+ density than socially housed mice in both of the pharmacological treatment groups, but not in the saline group. Drug treatment but not housing condition had strong effects on the behaviors of grooming, digging, rearing, and movement. Once the effects of drug condition were controlled, there were no across-individual correlations between cFos+ densities and behaviors. These findings suggest that the responses of auditory neurons to neuromodulation by serotonin are influenced by early life experience. 
    more » « less
  4. ; ; (, Frontiers in Neuroscience)
    Variation in the mutual responsiveness of social partners to each other can be reflected in behavioral suites that covary with neural activity in ways that track the salience or valence of interactions. Juvenile social isolation alters social behavior and neural activity during social interaction, but whether and how it alters the covariation between behavior and neural activity has not been as well explored. To address this issue, four classes of experimental subjects: isolated males, socially housed males, isolated females, and socially housed females, were paired with an opposite-sex social partner that had been socially housed. Social behaviors and c-Fos expression in the serotonergic dorsal raphe nucleus (DRN) were then measured in subjects following the social interactions. Relative to social housing, postweaning isolation led to a decrease in the density of neurons double-labeled for tryptophan hydroxylase and c-Fos in the dorsomedial subdivision of the DRN, regardless of sex. Vocal and non-vocal behaviors were also affected by isolation. In interactions with isolated males, both ultrasonic vocalization (USVs) and broadband vocalizations (squeaks) increased in conjunction with greater male investigation of females. Neural and behavioral measures also correlated with each other. In the isolated male group, the density of double-labeled neurons in the dorsomedial DRN was negatively correlated with USV production and positively correlated with a principal component of non-vocal behavior corresponding to greater defensive kicking by females and less investigation and mounting behavior. This correlation was reversed in direction for socially housed males, and for isolated males versus isolated females. These findings confirm that the dynamics of social interactions are reflected in c-Fos activation in the dorsomedial DRN, and suggest an altered responsiveness of serotonergic neurons to social interaction following social isolation in males, in parallel with an altered male response to female cues. 
    more » « less
  5. ; ; ; ; ; (, Physiology & Behavior)
    The neuropeptide, arginine vasopressin (AVP), has been implicated in social communication across a diverse array of species. Many rodents communicate basic behavioral states with negative versus positive valence through high-pitched vocalizations above the human hearing range (ultrasonic vocalizations; USVs). Previous studies have found that Brattleboro (Bratt) rats, which have a mutation in the Avp gene, exhibit deficits in their USVs from the early postnatal period through adolescence, but the magnitude of this effect appears to decrease from the juvenile to adolescent phase. The present study tested whether Bratt rats continue to exhibit USV deficits in adulthood. USVs of adult male and female Bratt and wild type (WT) rats were recorded in two contexts: a novel environment (empty arena) and a social context (arena filled with bedding soiled by same-sex conspecifics). The number, frequency, and duration of 50 kHz USVs were quantified by DeepSqueak after validation with manual scoring. Twenty-two kHz measures were quantified by manual scoring because DeepSqueak failed to accurately detect USVs in this frequency range. Adult Bratt rats did not exhibit deficits in the number of 50 kHz USVs: male Bratt rats emitted similar 50 kHz USVs as male WT rats, whereas female Bratt rats emitted more USVs than female WT rats. USV frequency and duration were altered in adult Bratt rats, but in a context-dependent manner. Twenty-two kHz USVs were less affected by the Bratt mutation. The present study demonstrates how chronic AVP deficiency impacts social communication across the lifespan. The present findings reveal a complex role for AVP in vocal communication, whereby disruption to the Avp gene leads to sex-, context-, and developmental phase-specific effects on the quantity and spectrotemporal characteristics of rat USVs. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email